Interpretive Summary: Striking losses of domesticated honey bees can be caused by poor nutrition, exposure to chemicals, and the effects of parasites and pathogens. Here we collected individual bees as they died, daily, from research colonies in Switzerland. Each bee was analyzed for the presence and levels of viruses and other pathogens, and colonies were scored for health as well as the presence of parasitic Varroa mites. The results indicate, for these bee colonies, that the virus Deformed wing virus is strongly tied with poor survivorship, along with levels of parasitic mites. The results strengthen arguments that the control of mites should be the primary concern of beekeepers as they maintain their colonies for pollination and honey production. This study aids research into bee health, and ultimately the bee industry, by pointing out threats in bee hives that are likely to cause colony collapse.

Technical Abstract:
Elevated winter losses of managed honey bee colonies are a major concern, but the underlying mechanisms remain controversial. Among suspects are the parasitic mite Varroa destructor, the microsporidian Nosema ceranae and associated viruses. Here, we hypothesize that pathogens reduce the life expectancy of winter bees and consequently of colonies. A monitoring of colonies was performed over six months in Switzerland from summer 2007 to winter 2007/2008. Individual dead workers were collected daily and quantitatively analyzed for deformed wing virus (DWV), acute bee paralysis virus (ABPV), N. ceranae and expression levels of the vitellogenin gene as a biomarker for honey bee longevity. Workers from colonies not surviving winter had a reduced life span, were more likely to be infected with DWV and had higher DWV loads. Colony levels of infection with the parasitic mite Varroa destructor and individual infections with DWV were also associated with reduced honey bee life expectancy. In sharp contrast, the level of N. ceranae infection was not correlated with longevity. In addition, vitellogenin gene expression was significantly positively correlated with ABPV and N. ceranae loads. Our findings strongly suggest that V. destructor and DWV but neither N. ceranae nor ABPV reduce life span of winter bees, thereby constituting a parsimonious mechanism for colony losses.